We have described the oral status and salivary flow rate of 30 children and adolescents suffering from chronic renal failure (CRF) undergoing hemodialysis and compared the associated parameters with those of 30 clinically healthy subjects with no history of chronic disease. The subjects of the renal group (RG) and healthy group (HG) were paired by gender and age (7–19 years old). Anamneses and an interview consisting of questions on oral hygiene habits comprised the first step in the study, followed by whole and parotid saliva collection and intra-oral examination. No statistical significant difference was found between the RG and HG subjects in terms of the presence of gingival inflammation, dental history of caries, and enamel hypoplasia. However, statistical significant differences were found between the groups related to a sensation of dry mouth, salivary flow rate, delayed tooth eruption, dental staining by iron supplementation, presence of plaque, and dental calculus. Based on our results, we conclude that CRF children and adolescents undergoing hemodialysis present some oral manifestations related to their disease. These manifestations include a sensation of dry mouth, delayed tooth eruption, dental staining by iron supplementation, and dental calculus. A lower flow rate of whole and parotid saliva production just before hemodialysis was also observed.
Chronic renal failure (CRF) is a progressive and irreversible decline in renal function associated with a reduced glomerular filtration rate [1, 2]. In addition to the systemic manifestations that appear due to CRF, the metabolic and pathophysiological changes associated with the disease and its treatment modalities can affect the oral cavity [2, 3]. These effects include pale oral mucosa, enamel hypoplasia [4–6], gingival inflammation [5, 7], gingival overgrowth, periodontal attachment loss, pulpal obliteration , low prevalence of dental caries [4, 5, 8–10], dry mouth, uremic odor, change in taste , high prevalence of dental calculus [8, 11], low salivary flow rate [4, 11, 12], and altered salivary composition [11–14].
Given the increasing number of children and adolescents suffering from CRF and the complications that arise from the disease and its treatment, oral manifestations are of great interest to dental professionals, mainly because oral health is an important factor influencing morbidity and the final stage of renal disease. Treatment can be drastically delayed in cases of unsatisfactory oral health; for example, a transplantation procedure can be postponed if an individual presents an unsatisfactory oral health status (because of the possibility of post-surgery infection). As such, an acceptable health status must be established prior to consideration for transplantation [9, 15]. However, the oral manifestation of CRF is not easily recognized by many dental  and medical professionals, and the attention given to dental care by such professionals seems to be unsatisfactory .
The aim of the study reported here was to describe the oral status and salivary flow rate of CRF children and adolescents undergoing hemodialysis and compare these parameters of oral health with those of healthy subjects.
Materials and methods
After receiving the approval of the Local Ethics Committee for this study, we selected 30 Brazilian children and adolescents of both genders, aged 7–19 years, who had been diagnosed with CRF and were currently undergoing hemodialysis in nine different Nephrology Services (Rio de Janeiro, Brazil) to form the Renal Group (RG). The Healthy Group (HG) consisted of 30 clinically healthy Brazilian children and adolescents with no history of chronic illness – in particular, no history of renal disease – who presented themselves for dental treatment at the Dental School of a public university in Rio de Janeiro, Brazil. The patients of the HG were matched with those of the RG in terms of age and gender. Those subjects (from both groups) who were receiving orthodontic treatment were excluded.
Anamnesis was performed and, with respect to the subjects of the RG, information on the time of diagnosis of CRF and drugs administrated were gathered from medical records. A clinical questionnaire (previously tested) was used to obtain information on oral hygiene habits, frequency of the habits, if the child/adolescent had already visited the dentist, how old he/she was at the first visit to the dentist, and when he/she had last visited the dentist. The subject was also asked if he/she had experienced a sensation of a dry mouth. Patients from the HG who were on drug therapy (receiving any kind of drug) were excluded from the study. The drugs listed by each patients in the RG were investigated in order to determine whether they were able to produce xerostomic effects or a reduction of the salivary flow rate, which could justify the sensation of dry mouth.
Stimulated whole saliva and parotid saliva were collected to determine the salivary flow rate. The saliva of the subjects of the RG was collected during two time intervals, one just prior to the hemodialysis (RG-T1) and the second collection following hemodialysis (RG-T2). Whole saliva was stimulated by chewing on a piece of Parafilm (10 × 10 cm, weighing 1.40 g), while parotid saliva was stimulated by applying a 2% citric acid solution onto the lateral border of the tongue for 30 s and collected from the right gland using a Lashley cup. Both salivary collections were performed for 5 min, and the saliva secreted in the first 30 s was discarded. The salivary flow rate (ml/min) was calculated soon after the collection.
The intra-oral exam included the Plaque Index System  and Gingival Index System  to evaluate, respectively, the presence of dental plaque and gingival condition. The Volpe–Manhold (VM) method was also applied , which measures calculus deposition on the lingual surface of the lower incisors by bisecting the surfaces with a periodontal probe and recording the calculus heights in millimeters. Based on the rate of calculus deposition (mm/tooth) determined by the VM method, the subjects were classified as light (<0.5 mm/tooth), moderate (0.6-1.5 mm/tooth), or heavy (>1.5 mm/tooth) calculus former, as suggested by Epstein et al. . Dental caries in permanent teeth were diagnosed by visual examination with a probe and dental mirror, and the DMF-T Index was established in accordance with the criteria suggested by the World Health Organization . A radiographic exam was not performed.
Tooth eruption was considered to be delayed when there was a delay of more than 6 months in comparison with the normal period of eruption and, as such, not in correspondence with the child’s chronological age, according to McCall and Wald . Enamel hypoplasia, which consists of a defect involving the enamel surface associated with a reduced localized thickness of enamel (that may be translucent or opaque) , was recorded when present on at least one tooth. The same criterium was used for the cases of teeth stained by oral iron supplementation.
All stages of data collection were performed by the same examiner, who had been previously trained to perform the VM method (intra-class correlation = 0.99). Written informed consent was obtained from all caregivers and verbal consent from the children/adolescents. All subjects and their guardians were informed about the oral treatment needs and referred to the Dental School of the same public university cited above.
The software SPSS ver. 11.0 (SPSS, Chicago, IL) was applied and the statistical significance of the difference between RG and HG was analyzed using the Mann-Whitney test for quantitative variables based on mean, minimum, and maximum values observed. The χ2 test was used for qualitative variables, and the Wilcoxon test was applied to analyze the statistical significance of the difference between RG-T1 and RG-T2.
There were no statistically signficant differences in terms of age and gender between the subjects of the RG and those in the HG (Table 1). The mean time between diagnosis of CRF and examination was 78.63 ± 61.86 months (range 6–200 months), while the mean age at CRF diagnosis was 8.33 ± 5.22 years (range 0–17 years) (Table 2). Four (13.3%) subjects in the RG were diagnosed with CRF at birth. The subjects in the RG had undergone hemodialysis for a mean of 32.66 months (range 1–120 months). All subjects in the RG were receiving some form of drug therapy.
There was no statistically significant difference between the groups in terms of oral hygiene habits. In the HG group, 90.0% of the subjects had visited a dentist, while only 76.6% of those of the RG group has visited a dentist; however, this difference was not statistically significant (χ2, p > 0.01). The mean age of the subjects at the time of their first visit to a dentist was 8.7 years for the RG group (range 3–16 years) and 5.6 years (range 1–11) for the HG (t test, p > 0.01). Only eight subject (26.6%) from the RG had visited the dentist within the past year compared to 21 (70%) from the HG (χ2, p ≤ 0.05).
The flow rate of whole saliva and parotid saliva is shown in Table 3. There was a positive correlation between stimulated whole saliva flow rate in RG-T2 and stimulated parotid secretion flow rate in RG-T2 (r = 0.75, p < 0.05). No statistically significant difference was found when the sensation of dry mouth was compared with either the administration of a xerostomic drug (such as furosemide and oxybutynin chloride) or the salivary flow rate of whole and parotid saliva.
The findings on oral manifestations are given in Table 4 and the Plaque and Gingival indices are given in Table 5. The DMF-T values ranged from 0 to 12 (mean 1.66) and from 0 to 9 (1.93) in the RG and HG, respectively (t test, p > 0.05). Sixteen (53.3%) subjects from the RG and 13 (43.3%) from the HG had no caries experience (DMF-T = 0), but this difference was not statically significant (χ2, p > 0.05). However, all four subjects from the RG who were diagnosed with CRF at birth had a DMF-T equal to zero.
In terms of dental calculus, based on the VM method, the RG subjects presented a mean value of 5.14 mm/tooth (range 0–17.16 mm/tooth), while those in the HG presented a mean value of 1.16 mm/tooth (range 0–7.3 mm/tooth) (t test, p < 0.001). A statistically significant difference between the RG and HG subjects was also observed after they had been classified as light, moderate or heavy calculus formers (Table 6). No statistical significance was noted between the presence of plaque and dental calculus in the RG (χ2, p > 0.05).
Although infrequent oral hygiene habits associated with CRF have been reported in the literature , we found that our RG and HG subjects had similar oral hygiene habits (p > 0.05). In contrast, when the subjects were questioned about their previous visit to a dentist, a statistically significant difference was found between the groups, which is in accordance with results published earlier . This result suggests that priority must have being given to the general health care of these children and that the importance of oral health care should be emphasized. It is quite understandable that the RG subjects undergoing hemodialysis, who have a strict treatment routine, have less time than their healthy counterparts to undergo any treatment for their oral ailments. This lack of time may be the reason why so few subjects from the RG had visited a dentist during the year preceding this study. However, other factors, such as economical difficulties, lack of motivation, and stress, may also impede visits to a dentist.
Saliva was collected from the subjects in the RG before and after hemodialysis, based on Martins et al. , who observed a statistically significant difference between these two moments of measurement. Although variations in the stimulated salivary flow rate during the day have been observed in earlier studies , we did not observed any such difference at these different periods. In terms of parotid saliva flow rate, some authors [7, 11] have suggested that subjects with CRF may have a lower salivary secretion due to altered gland function; however, we did not find any difference between HG and RG-T2 in terms of parotid saliva flow rate. This result is in agreement with results reported in the literature  which show that salivary glands of subjects undergoing hemodialysis function normally and are apparently unimpaired by the metabolic changes occurring due to both renal disease and its treatment. This result is supported by the positive correlation between stimulated whole saliva flow rate in RG-T2 and stimulated parotid secretion flow rate in RG-T2. However, a significant difference can be noted when the parotid saliva flow rate in HG is compared to RG-T1; the same is true for the whole saliva.
The whole saliva flow rate was found to be lower in the RG-T1, thus corroborating previous findings  from a salivary analysis of adult patients undergoing hemodialysis. However, in both studies, the whole saliva flow rate increased after the hemodialysis, becoming similar to that of healthy subjects. It has been suggested that a systemic involvement of subjects undergoing hemodialysis could be affecting the salivary flow rate and that the therapy is able to reestablish the normal rate.
A sensation of dry mouth is a common oral symptom of CRF, which may be caused by restricted fluid intake (necessary to accommodate the reduced excretory capacity of the kidney), adverse effects of drug therapy, low salivary flow rate, and/or mouth-breathing [2, 6, 17]. However, our results support those of previous studies in showing the absence of an association between the sensation of dry mouth and the administration of drugs that could promote such a side-effect, or flow rate of whole saliva and parotid saliva. The sensation of dry mouth has been attributed to a restricted fluid intake by some subjects in the anamneses.
Despite the increased prevalence of enamel hypoplasia in subjects suffering from CRF, as reported in the literature [4, 8], Kho et al.  observed that enamel hypoplasia was rare in subjects with CRF. The result of these researchers can possibly be attributed to the age of the subjects in their study (mean age 33.5 years) and to represent a possible CRF manifestation after crown development of the teeth . We also did not find a higher prevalence of enamel hypoplasia in CRF patients (RG) than in healthy subjects (HG) among our study cohort of children and adolescents. However, we should point out that a wide range of enamel defects appeared in the subjects of the RG, ranging from white opacities to morphologic anomalies, while only mild opacities in isolated teeth were identified in the subjects of the HG. The fact that maxillary anterior teeth were mostly involved suggests that, in the HG subjects, the enamel hypoplasia may have been caused by dental traumatism .
The high prevalence of delayed tooth eruption and dental staining due to the administration of oral iron supplementation for treating anemia (which is a common systemic manifestation of CRF), both experienced by patients in the RG, corroborates previous studies [1, 10]. Nevertheless, although subjects suffering from CRF require a diet with an increased intake of carbohydrates to compensate for the reduced calories from a protein-sparing diet aimed at minimizing nitrogenous waste products [2, 3], a low prevalence of dental caries has been observed in these subjects [4, 5, 8–10], which may result from increases in the salivary urea concentration and a high salivary buffering capacity in patients with CRF [4, 5]. However, although we found that while the prevalence of dental caries was lower in the subjects of the RG, it was not significantly different than that found for the subject of the HG, possibly because previous caries experience before the development of the renal disease in the former. This possibility is emphasized when all the subjects diagnosed with CRF at birth were found to have DMF-T equal to zero (p < 0.05). Furthermore, only one patient from RG who had DMF-T different from zero presented active caries lesion.
In agreement with results reported in the literature [4, 5, 7, 17, 26], the presence of plaque was higher in RG subjects, which reflects an inadequate oral hygiene; however, when compared with the presence of plaque in the HG, this difference was not statistically significant. Based on the answers given during anamnesis, the subjects from the RG seemed to have oral hygiene habits that were similar to those of the HG subjects (p > 0.05). The increased plaque scores in subjects with CRF can be due to the importance given to general medical care for a chronic disease and prolonged hospitalizations as well as by the effect of the former on the subjects’ lifestyle [4, 5]. It is also important to remember that enamel hypoplasia can also contribute to plaque accumulation, especially if the marginal gingiva is affected.
The results observed in relation to gingival inflammation and the lack of association between plaque and gingival inflammation corroborate the results of a previous study  in which little periodontal disease or gingival inflammation in children with CRF was observed. This reduced gingival inflammatory response to dental plaque, which subjects suffering from CRF seem to present with, can be attributed to a modified tissue response as a result of systemic involvement. Furthermore, gingival inflammation can be masked by the paleness of gingivae due to anemia .
It is important that subjects and guardians be informed about the role of oral hygiene in reducing the risk of oral infections and, consequently, eliminate the risk of septicemia, endocarditis, and other possible infections which can lead to serious health consequences in subjects with CRF. In renal transplant subjects, the immunosuppressive drugs prescribed may further predispose to disseminated infections . Therefore, the incorporation of dental treatment protocols would benefit the patients .
The high prevalence of dental calculus among our RG subjects corroborates reported findings [8, 11], but in our study there was no association between calculus and plaque or gingival inflammation, indicating that an unknown causative agent could be associated with calculus formation in subjects with CRF. We therefore recommend that studies focusing on the factors which influence calculus formation during CRF are necessary to help establish a periodontal protocol for these subjects.
Based on the findings of our study, we conclude that children and adolescents suffering from CRF present oral manifestations associated with the disease as well as a stronger dental calculus accumulation that was not associated with dental plaque. An altered salivary flow rate just before the hemodialysis was also observed. It is therefore necessary to establish a periodic dental protocol for these subjects in order to improve their oral status.
Chan JC, Williams DM, Roth KS (2002) Kidney failure in infants and children. Pediatr Rev 23:47–60
Proctor R, Kumar N, Stein A, Moles D, Porter S (2005) Oral and dental aspects of chronic renal failure. J Dent Res 84:199–208
Lucas VS, Roberts GJ (2005) Oro-dental health in children with chronic renal failure and after renal transplantation: a clinical review. Pediatr Nephrol 20:1388–1394
Al-Nowaiser A, Roberts GJ, Trompeter RS, Wilson M, Lucas VS (2003) Oral health in children with chronic renal failure. Pediatr Nephrol 18:39–45
Davidovich E, Schwarz Z, Davidovitch M, Eidelman E, Bimstein E (2005) Oral findings and periodontal status in children, adolescents and young adults suffering from renal failure. J Clin Periodontol 32:1076–1082
Kho HS, Lee SW, Chung SC, Kim YK (1999) Oral manifestations and salivary flow rate, pH, and buffer capacity in patients with end-stage renal disease undergoing hemodialysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 88:316–319
Gavalda C, Bagan J, Scully C, Silvestre F, Milian M, Jimenez Y (1999) Renal hemodialysis patients: oral, salivary, dental and periodontal findings in 105 adult cases. Oral Dis 5:299–302
Jaffe EC, Roberts GJ, Chantler C, Carter JE (1986) Dental findings in chronic renal failure. Br Dent J 160:18–20
Naugle K, Darby ML, Bauman DB, Lineberger LT, Powers R (1998) The oral health status of individuals on renal dialysis. Ann Periodontol 3:197–205
Wolff A, Stark H, Sarnat H, Binderman I, Eisenstein B, Drukker A (1985) The dental status of children with chronic renal failure. Int J Pediatr Nephrol 6:127–132
Epstein SR, Mandel I, Scopp IW (1980) Salivary composition and calculus formation in patients undergoing hemodialysis. J Periodontol 51:336–338
Martins C, Siqueira WL, Primo LG, Oliveira E, Nicolau J (2006) Salivary analysis of patients with chronic renal failure undergoing hemodialysis. Spec Care Dentist 26:205–208
Obry F, Belcourt AB, Frank RM, Geisert J, Fischbach M (1987) Biochemical study of whole saliva from children with chronic renal failure. ASDC J Dent Child 54:429–432
Peterson S, Woodhead J, Crall J (1985) Caries resistance in children with chronic renal failure: plaque pH, salivary pH, and salivary composition. Pediatr Res 19:796–799
Marakoglu I, Gursoy UK, Demirer S, Sezer H (2003) Periodontal status of chronic renal failure patients receiving hemodialysis. Yonsei Med J 44:648–652
Martins C, Binato J, Primo LG (2004) Management of patients with CRF: perception of students and lectures. J Dent Res 83 (Spec Issue A), no.1992. Available at: https://doi.org/www.dentalresearch.org
Klassen JT, Krasko BM (2002) The dental health status of dialysis patients. J Can Dent Assoc 68:34–38
Silness J, Löe H (1964) Periodontal disease in pregnancy. II Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135
Löe H, Silness J (1963) Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 21:533–551
Volpe AR, Manhold JH, Hazen SP (1965) In vivo calculus assessment. I. A method and its examiner reproducibility. J Periodontol 36:292–298
World Health Organization (1987) Oral health survey, basic methods, 3rd edn. World Health Organization, Geneva
McCall JO, Wald SS (1940) Clinical dental roentgenology: technic and interpretation including roentgen studies of the child and young adult. W.B.Saunders, Philadelphia, pp 96–103
FDI Commission on Oral Health, Research and Epidemiology (1992) A review of the developmental defects of enamel index (DDE Index). Int Dent J 42:411–426
Ghezzi EM, Lange LA, Ship JA (2000) Determination of variation of stimulated salivary flow rates. J Dent Res 79:1874–1878
Dahlberg WH, Sreebny LM, King B (1967) Studies of parotid saliva and blood in hemodialysis patients. J Appl Physiol 23:100–108
Rahman MM, Caglayan F, Rahman B (1992) Periodontal health parameters in patients with chronic renal failure and renal transplants receiving immunosuppressive therapy. J Nihon Univ Sch Dent 34:265–272
The authors are grateful to the Fundação do Rim Francisco Santino Filho for helping to localize the Nephrology Services where children and adolescents were treated and also to the nephrologists, particularly, Dr. Arnauld Kaufman, for allowing us to study the subjects’ medical charts.
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Martins, C., Siqueira, W.L. & Guimarães Primo, L.S.S. Oral and salivary flow characteristics of a group of Brazilian children and adolescents with chronic renal failure. Pediatr Nephrol 23, 619–624 (2008). https://doi.org/10.1007/s00467-007-0718-5
- Chronic kidney failure
- Clinical features
- Dental care
- Oral health
- Salivary flow rate